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      Neonatal White Matter Maturation Is Associated With Infant Language Development

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          Abstract

          Background

          While neonates have no sophisticated language skills, the neural basis for acquiring this function is assumed to already be present at birth. Receptive language is measurable by 6 months of age and meaningful speech production by 10–18 months of age. Fiber tracts supporting language processing include the corpus callosum (CC), which plays a key role in the hemispheric lateralization of language; the left arcuate fasciculus (AF), which is associated with syntactic processing; and the right AF, which plays a role in prosody and semantics. We examined if neonatal maturation of these fiber tracts is associated with receptive language development at 12 months of age.

          Methods

          Diffusion-weighted imaging (DWI) was performed in 86 infants at 26.6 ± 12.2 days post-birth. Receptive language was assessed via the MacArthur-Bates Communicative Development Inventory at 12 months of age. Tract-based fractional anisotropy (FA) was determined using the NA-MIC atlas-based fiber analysis toolkit. Associations between neonatal regional FA, adjusted for gestational age at birth and age at scan, and language development at 12 months of age were tested using ANOVA models.

          Results

          After multiple comparisons correction, higher neonatal FA was positively associated with receptive language at 12 months of age within the genu ( p < 0.001), rostrum ( p < 0.001), and tapetum ( p < 0.001) of the CC and the left fronto-parietal AF ( p = 0.008). No significant clusters were found in the right AF.

          Conclusion

          Microstructural development of the CC and the AF in the newborn is associated with receptive language at 12 months of age, demonstrating that interindividual variation in white matter microstructure is relevant for later language development, and indicating that the neural foundation for language processing is laid well ahead of the majority of language acquisition. This suggests that some origins of impaired language development may lie in the intrauterine and potentially neonatal period of life. Understanding how interindividual differences in neonatal brain maturity relate to the acquisition of function, particularly during early development when the brain is in an unparalleled window of plasticity, is key to identifying opportunities for harnessing neuroplasticity in health and disease.

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          Most cited references 56

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          Differences in white matter fiber tract development present from 6 to 24 months in infants with autism.

          Evidence from prospective studies of high-risk infants suggests that early symptoms of autism usually emerge late in the first or early in the second year of life after a period of relatively typical development. The authors prospectively examined white matter fiber tract organization from 6 to 24 months in high-risk infants who developed autism spectrum disorders (ASDs) by 24 months. The participants were 92 high-risk infant siblings from an ongoing imaging study of autism. All participants had diffusion tensor imaging at 6 months and behavioral assessments at 24 months; a majority contributed additional imaging data at 12 and/or 24 months. At 24 months, 28 infants met criteria for ASDs and 64 infants did not. Microstructural properties of white matter fiber tracts reported to be associated with ASDs or related behaviors were characterized by fractional anisotropy and radial and axial diffusivity. The fractional anisotropy trajectories for 12 of 15 fiber tracts differed significantly between the infants who developed ASDs and those who did not. Development for most fiber tracts in the infants with ASDs was characterized by higher fractional anisotropy values at 6 months followed by slower change over time relative to infants without ASDs. Thus, by 24 months of age, those with ASDs had lower values. These results suggest that aberrant development of white matter pathways may precede the manifestation of autistic symptoms in the first year of life. Longitudinal data are critical to characterizing the dynamic age-related brain and behavior changes underlying this neurodevelopmental disorder.
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            Unbiased diffeomorphic atlas construction for computational anatomy.

            Construction of population atlases is a key issue in medical image analysis, and particularly in brain mapping. Large sets of images are mapped into a common coordinate system to study intra-population variability and inter-population differences, to provide voxel-wise mapping of functional sites, and help tissue and object segmentation via registration of anatomical labels. Common techniques often include the choice of a template image, which inherently introduces a bias. This paper describes a new method for unbiased construction of atlases in the large deformation diffeomorphic setting. A child neuroimaging autism study serves as a driving application. There is lack of normative data that explains average brain shape and variability at this early stage of development. We present work in progress toward constructing an unbiased MRI atlas of 2 years of children and the building of a probabilistic atlas of anatomical structures, here the caudate nucleus. Further, we demonstrate the segmentation of new subjects via atlas mapping. Validation of the methodology is performed by comparing the deformed probabilistic atlas with existing manual segmentations.
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              A longitudinal study of the relation between language and theory-of-mind development.

              Fifty-nine 3-year-olds were tested 3 times over a period of 7 months in order to assess the contribution of theory of mind to language development and of language to theory-of-mind development (including the independent contributions of syntax and semantics). Language competence was assessed with a standardized measure of reception and production of syntax and semantics (the Test of Early Language Development). Theory of mind was assessed with false-belief tasks and appearance-reality tasks. Earlier language abilities predicted later theory-of-mind test performance (controlling for earlier theory of mind), but earlier theory of mind did not predict later language test performance (controlling for earlier language). These findings are consistent with the argument that language is fundamental to theory-of-mind development.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                17 December 2019
                2019
                : 13
                Affiliations
                1Department of Medical Psychology, Berlin Institute of Health, Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin , Berlin, Germany
                2Department of Psychiatry, University of North Carolina at Chapel Hill , Chapel Hill, NC, United States
                3Development, Health, and Disease Research Program, University of California , Irvine, Orange, CA, United States
                Author notes

                Edited by: Christian K. Tamnes, University of Oslo, Norway

                Reviewed by: Claire Kelly, Murdoch Childrens Research Institute (MCRI), Australia; Stine Kleppe Krogsrud, University of Oslo, Norway

                *Correspondence: Claudia Buss, claudia.buss@ 123456charite.de

                This article was submitted to Speech and Language, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2019.00434
                6927985
                Copyright © 2019 Sket, Overfeld, Styner, Gilmore, Entringer, Wadhwa, Rasmussen and Buss.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 2, Tables: 3, Equations: 0, References: 69, Pages: 11, Words: 0
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: R01 MH-091351
                Award ID: R01 MH-105538
                Award ID: R01 HD-060628
                Award ID: UG3 OD-O23349
                Categories
                Neuroscience
                Original Research

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